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1. Feedback Regulation between Aquatic Microorganisms and the Bloom-Forming Cyanobacterium Microcystis aeruginosa

   https://doi.org/10.1128/AEM.01362-19  

   Zhang, Meng ; Lu, Tao ; Paerl, Hans W. ; Chen, Yiling ; Zhang, Zhenyan ; Zhou, Zhigao ; Qian, Haifeng ; Drake, Harold L. ( November 2019 , Applied and Environmental Microbiology)

   ABSTRACT The frequency and intensity of cyanobacterial blooms are increasing worldwide. Interactions between toxic cyanobacteria and aquatic microorganisms need to be critically evaluated to understand microbial drivers and modulators of the blooms. In this study, we applied 16S/18S rRNA gene sequencing and metabolomics analyses to measure the microbial community composition and metabolic responses of the cyanobacterium Microcystis aeruginosa in a coculture system receiving dissolved inorganic nitrogen and phosphorus (DIP) close to representative concentrations in Lake Taihu, China. M. aeruginosa secreted alkaline phosphatase using a DIP source produced by moribund and decaying microorganisms when the P source was insufficient. During this process, M. aeruginosa accumulated several intermediates in energy metabolism pathways to provide energy for sustained high growth rates and increased intracellular sugars to enhance its competitive capacity and ability to defend itself against microbial attack. It also produced a variety of toxic substances, including microcystins, to inhibit metabolite formation via energy metabolism pathways of aquatic microorganisms, leading to a negative effect on bacterial and eukaryotic microbial richness and diversity. Overall, compared with the monoculture system, the growth of M. aeruginosa was accelerated in coculture, while the growth of some cooccurring microorganisms was inhibited, with the diversity and richness of eukaryoticmore »microorganisms being more negatively impacted than those of prokaryotic microorganisms. These findings provide valuable information for clarifying how M. aeruginosa can potentially modulate its associations with other microorganisms, with ramifications for its dominance in aquatic ecosystems. IMPORTANCE We measured the microbial community composition and metabolic responses of Microcystis aeruginosa in a microcosm coculture system receiving dissolved inorganic nitrogen and phosphorus (DIP) close to the average concentrations in Lake Taihu. In the coculture system, DIP is depleted and the growth and production of aquatic microorganisms can be stressed by a lack of DIP availability. M. aeruginosa could accelerate its growth via interactions with specific cooccurring microorganisms and the accumulation of several intermediates in energy metabolism-related pathways. Furthermore, M. aeruginosa can decrease the carbohydrate metabolism of cooccurring aquatic microorganisms and thus disrupt microbial activities in the coculture. This also had a negative effect on bacterial and eukaryotic microbial richness and diversity. Microcystin was capable of decreasing the biomass of total phytoplankton in aquatic microcosms. Overall, compared to the monoculture, the growth of total aquatic microorganisms is inhibited, with the diversity and richness of eukaryotic microorganisms being more negatively impacted than those of prokaryotic microorganisms. The only exception is M. aeruginosa in the coculture system, whose growth was accelerated.« less
2. Bioavailable iron titrations reveal oceanic Synechococcus ecotypes optimized for different iron availabilities

   https://doi.org/10.1038/s43705-022-00132-5  

   Gilbert, Naomi E. ; LeCleir, Gary R. ; Strzepek, Robert F. ; Ellwood, Michael J. ; Twining, Benjamin S. ; Roux, S. ; Pennacchio, C. ; Boyd, Philip W. ; Wilhelm, Steven W. ( July 2022 , ISME Communications)

   The trace metal iron (Fe) controls the diversity and activity of phytoplankton across the surface oceans, a paradigm established through decades of in situ and mesocosm experimental studies. Despite widespread Fe-limitation within high-nutrient, low chlorophyll (HNLC) waters, significant contributions of the cyanobacteriumSynechococcusto the phytoplankton stock can be found. Correlations among differing strains ofSynechococcusacross different Fe-regimes have suggested the existence of Fe-adapted ecotypes. However, experimental evidence of high- versuslow-Fe adapted strains ofSynechococcusis lacking, and so we investigated the transcriptional responses of microbial communities inhabiting the HNLC, sub-Antarctic region of the Southern Ocean during the Spring of 2018. Analysis of metatranscriptomes generated from on-deck incubation experiments reflecting a gradient of Fe-availabilities reveal transcriptomic signatures indicative of co-occurringSynechococcusecotypes adapted to differing Fe-regimes. Functional analyses comparing low-Fe and high-Fe conditions point to various Fe-acquisition mechanisms that may allow persistence of low-Fe adaptedSynechococcusunder Fe-limitation. Comparison of in situ surface conditions to the Fe-titrations indicate ecological relevance of these mechanisms as well as persistence of both putative ecotypes within this region. This Fe-titration approach, combined with transcriptomics, highlights the short-term responses of the in situ phytoplankton community to Fe-availability that are often overlooked by examining genomic content or bulk physiological responses alone. These findings expandmore »our knowledge about how phytoplankton in HNLC Southern Ocean waters adapt and respond to changing Fe supply.

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3. Organismal and cellular interactions in vertebrate–alga symbioses

   https://doi.org/10.1042/BST20210153  

   Yang, Hui ; Genot, Baptiste ; Duhamel, Solange ; Kerney, Ryan ; Burns, John A. ( February 2022 , Biochemical Society Transactions)

   Photosymbioses, intimate interactions between photosynthetic algal symbionts and heterotrophic hosts, are well known in invertebrate and protist systems. Vertebrate animals are an exception where photosynthetic microorganisms are not often considered part of the normal vertebrate microbiome, with a few exceptions in amphibian eggs. Here, we review the breadth of vertebrate diversity and explore where algae have taken hold in vertebrate fur, on vertebrate surfaces, in vertebrate tissues, and within vertebrate cells. We find that algae have myriad partnerships with vertebrate animals, from fishes to mammals, and that those symbioses range from apparent mutualisms to commensalisms to parasitisms. The exception in vertebrates, compared with other groups of eukaryotes, is that intracellular mutualisms and commensalisms with algae or other microbes are notably rare. We currently have no clear cell-in-cell (endosymbiotic) examples of a trophic mutualism in any vertebrate, while there is a broad diversity of such interactions in invertebrate animals and protists. This functional divergence in vertebrate symbioses may be related to vertebrate physiology or a byproduct of our adaptive immune system. Overall, we see that diverse algae are part of the vertebrate microbiome, broadly, with numerous symbiotic interactions occurring across all vertebrate and many algal clades. These interactions are being studiedmore »for their ecological, organismal, and cellular implications. This synthesis of vertebrate–algal associations may prove useful for the development of novel therapeutics: pairing algae with medical devices, tissue cultures, and artificial ecto- and endosymbioses.« less
4. Potential virus-mediated nitrogen cycling in oxygen-depleted oceanic waters

   https://doi.org/10.1038/s41396-020-00825-6  

   Gazitúa, M. Consuelo ; Vik, Dean R. ; Roux, Simon ; Gregory, Ann C. ; Bolduc, Benjamin ; Widner, Brittany ; Mulholland, Margaret R. ; Hallam, Steven J. ; Ulloa, Osvaldo ; Sullivan, Matthew B. ( November 2020 , The ISME Journal)

   Viruses play an important role in the ecology and biogeochemistry of marine ecosystems. Beyond mortality and gene transfer, viruses can reprogram microbial metabolism during infection by expressing auxiliary metabolic genes (AMGs) involved in photosynthesis, central carbon metabolism, and nutrient cycling. While previous studies have focused on AMG diversity in the sunlit and dark ocean, less is known about the role of viruses in shaping metabolic networks along redox gradients associated with marine oxygen minimum zones (OMZs). Here, we analyzed relatively quantitative viral metagenomic datasets that profiled the oxygen gradient across Eastern Tropical South Pacific (ETSP) OMZ waters, assessing whether OMZ viruses might impact nitrogen (N) cycling via AMGs. Identified viral genomes encoded six N-cycle AMGs associated with denitrification, nitrification, assimilatory nitrate reduction, and nitrite transport. The majority of these AMGs (80%) were identified in T4-likeMyoviridaephages, predicted to infectCyanobacteriaandProteobacteria, or in unclassified archaeal viruses predicted to infectThaumarchaeota. Four AMGs were exclusive to anoxic waters and had distributions that paralleled homologous microbial genes. Together, these findings suggest viruses modulate N-cycling processes within the ETSP OMZ and may contribute to nitrogen loss throughout the global oceans thus providing a baseline for their inclusion in the ecosystem and geochemical models.
5. Prochlorococcus Exudate Stimulates Heterotrophic Bacterial Competition with Rival Phytoplankton for Available Nitrogen

   https://doi.org/10.1128/mbio.02571-21  

   Calfee, Benjamin C. ; Glasgo, Liz D. ; Zinser, Erik R. ( February 2022 , mBio)

   Martiny, Jennifer B. (Ed.)

   ABSTRACT The marine cyanobacterium Prochlorococcus numerically dominates the phytoplankton community of the nutrient-limited open ocean, establishing itself as the most abundant photosynthetic organism on Earth. This ecological success has been attributed to lower cell quotas for limiting nutrients, superior resource acquisition, and other advantages associated with cell size reduction and genome streamlining. In this study, we tested the prediction that Prochlorococcus outcompetes its rivals for scarce nutrients and that this advantage leads to its numerical success in nutrient-limited waters. Strains of Prochlorococcus and its sister genus Synechococcus grew well in both mono- and cocultures when nutrients were replete. However, in nitrogen-limited medium, Prochlorococcus outgrew Synechococcus but only when heterotrophic bacteria were also present. In the nitrogen-limited medium, the heterotroph Alteromonas macleodii outcompeted Synechococcus for nitrogen but only if stimulated by the exudate released by Prochlorococcus or if a proxy organic carbon source was provided. Genetic analysis of Alteromonas suggested that it outcompetes Synechococcus for nitrate and/or nitrite, during which cocultured Prochlorococcus grows on ammonia or other available nitrogen species. We propose that Prochlorococcus can stimulate antagonism between heterotrophic bacteria and potential phytoplankton competitors through a metabolic cross-feeding interaction, and this stimulation could contribute to the numerical success of Prochlorococcus inmore »nutrient-limited regions of the ocean. IMPORTANCE In nutrient-poor habitats, competition for limited resources is thought to select for organisms with an enhanced ability to scavenge nutrients and utilize them efficiently. Such adaptations characterize the cyanobacterium Prochlorococcus , the most abundant photosynthetic organism in the nutrient-limited open ocean. In this study, the competitive superiority of Prochlorococcus over a rival cyanobacterium, Synechococcus , was captured in laboratory culture. Critically, this outcome was achieved only when key aspects of the open ocean were simulated: a limited supply of nitrogen and the presence of heterotrophic bacteria. The results indicate that Prochlorococcus promotes its numerical dominance over Synechococcus by energizing the heterotroph’s ability to outcompete Synechococcus for available nitrogen. This study demonstrates how interactions between trophic groups can influence interactions within trophic groups and how these interactions likely contribute to the success of the most abundant photosynthetic microorganism.« less